Theta-Contingent Trial Presentation Accelerates Learning Rate and Enhances Hippocampal Plasticity during Trace Eyeblink Conditioning

Behavioral Neuroscience

Volumn 118, Issue 2, 2004, Pages 403-411

  Griffin, Amy L ^a,b   Asaka, Yukiko ^a,c   Darling, Ryan D ^a   Berry, Stephen D ^a  

^a MIAMI UNIVERSITY   (United States)

^b BOSTON UNIVERSITY   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONDITIONING; CONTROLLED STUDY; EYELID REFLEX; FEMALE; HIPPOCAMPUS; HIPPOCAMPUS THETA RHYTHM; LEARNING; MALE; NERVE CELL PLASTICITY; NONHUMAN; RABBIT;

ANIMALS; BEHAVIOR, ANIMAL; BLINKING; CONDITIONING (PSYCHOLOGY); HIPPOCAMPUS; LEARNING; NEURONAL PLASTICITY; RABBITS; THETA RHYTHM; TIME FACTORS;

EID: 1842479429     PISSN: 07357044     EISSN: None     Source Type: Journal    
DOI: 10.1037/0735-7044.118.2.403     Document Type: Article

References (63)

1. Adey, W. R. (1966). Neurophysiological correlates of information transaction and storage in brain tissue. In E. Stellar & J. M. Sprague (Eds.), Progress in physiological psychology (Vol. 1, pp. 1-43). New York: Academic Press.
2. Akase, E., Alkon, D. L., & Disterhoft, J. F. (1989). Hippocampal lesions impair memory of short-delay conditioned eyeblink in rabbits. Behavioral Neuroscience, 103, 935-943.
3. Arnolds, D. E., Lopes da Silva, F., Aitink, J. W., Kamp, A., & Boeijinga, P. (1980). The spectral properties of hippocampal EEG related to behaviour in man. Electroencephalography and Clinical Neurology, 50, 324-328.
4. Asaka, Y., & Berry, S. D. (2004). [Age-related learning deficits: Reversal by a hippocampal theta-dependent brain-computer interface]. Unpublished raw data.
5. Asaka, Y., Griffin, A. L., & Berry, S. D. (2002). Reversible septal inactivation disrupts hippocampal slow-wave and unit activity and impairs trace conditioning in rabbits (Oryctolagus cuniculus). Behavioral Neuroscience, 116, 434-442.
6. Asaka, Y., Seager, M. A., Griffin, A. L., & Berry, S. D. (2000). Medial septal microinfusion of scopolamine disrupts hippocampal activity and trace jaw movement conditioning. Behavioral Neuroscience, 114, 1068-1077.
7. Bennett, T. L. (1969). The electrical activity of the hippocampus and processes of attention. In R. L. Isaacson & K. H. Pribram (Eds.), The hippocampus (Vol. 2, pp. 71-99). New York: Plenum Press.
8. Berger, T., Rinaldi, P., Weisz, D., & Thompson, R. F. (1983). Single-unit analysis of different hippocampal cell types during classical conditioning of the rabbit nictitating membrane response. Journal of Neurophysiology, 50, 1197-1219.
9. Berger, T. W., & Thompson, R. F. (1978). Neuronal plasticity in the limbic system during classical conditioning of the rabbit nictitating membrane response: I. The hippocampus. Brain Research, 145, 323-346.
10. Berry, S. D., & Seager, M. A. (2001). Hippocampal theta oscillations and classical conditioning. Neurobiology of Learning and Memory, 76, 298-313.
11. Berry, S. D., Seager, M. A., Asaka, Y., & Borgnis, R. A. (2000). Motivational issues in aversive and appetitive conditioning paradigms. In D. S. Woodruff-Pak & J. E. Steinmetz (Eds.), Classical conditioning (Vol. 2, pp. 287-312). Boston: Kluwer Academic.
12. Berry, S. D., & Swain, R. A. (1989). Water deprivation optimizes hippocampal activity and facilitates nictitating membrane conditioning. Behavioral Neuroscience, 103, 71-76.
13. Berry, S. D., & Thompson, R. F. (1978, June 16). Prediction of learning rate from the hippocampal electroencephalogram. Science, 200, 1298-1300.
14. Berry, S. D., & Thompson, R. F. (1979, July 13). Medial septal lesions retard classical conditioning of the nictitating membrane response in rabbits. Science, 205, 209-211.
15. Buszaki, G. (2002). Theta oscillations in the hippocampus. Neuron, 33, 325-340.
16. Caplan, J. B., Madsen, J. R., Raghavachari, S., & Kahana, M. J. (2001). Distinct patterns of brain oscillations underlie two basic parameters of human maze learning. Journal of Neurophysiology, 86, 368-380.
17. Clark, G. A., McCormick, D. A., Lavond, D. G., & Thompson, R. F. (1984). Effects of lesions of cerebellar nuclei on conditioned behavioral and hippocampal neuronal responses. Brain Research, 291, 125-136.
18. Dickson, C. T., Kirk, I. J., Oddie, S. D., & Bland, B. H. (1995). Classification of theta-related cells in the entorhinal cortex: Cell discharges are controlled by the ascending brainstem synchronizing pathway in parallel with hippocampal theta-related cells. Hippocampus, 5, 306-319.
19. Eichenbaum, H., Otto, T., & Cohen, N. J. (1992). The hippocampus: What does it do? Behavioral and Neural Biology, 57, 2-36.
20. Frank, L. M., Brown, E. N., & Wilson, M. A. (2001). A comparison of the firing properties of putative excitatory and inhibitory neurons from CA1 and the entorhinal cortex. Journal of Neurophysiology, 86, 2029-2040.
21. Girgis, M., & Shih-Chang, W. (1981). Stereotaxic atlas of the rabbit brain. St. Louis: Warren H. Green.
22. Givens, B. S., & Olton, D. S. (1990). Cholinergic and GABAergic modulation of medial septal area: Effect on working memory. Behavioral Neuroscience, 104, 849-855.
23. Gluck, M. A., & Meyers, C. E. (1997). Psychobiological models of hippocampal function in learning and memory. Annual Review of Psychology, 48, 481-514.
24. Gormezano, I. (1966). Classical conditioning. In J. B. Sidowski (Ed.), Experimental methods and instrumentation in psychology (pp. 385-420). New York: McGraw-Hill.
25. Gormezano, I., Prokasy, W. F., & Thompson, R. F. (Eds.). (1987). Classical conditioning (3rd ed.). Hillsdale, NJ: Erlbaum.
26. Green, J. D., & Arduini, A. (1954). Hippocampal electrical activity in arousal. Journal of Neurophysiology, 17, 533-557.
27. Hasselmo, M. E., Bodelon, C., & Wyble, B. P. (2002). A proposed function for hippocampal theta rhythm: Separate phases of encoding and retrieval enhance reversal of prior learning. Neural Computation, 14, 793-817.
28. Holscher, C., Anwyl, R., & Rowan, M. J. (1997). Stimulation on the positive phase of hippocampal theta rhythm induces long-term potentiation that can be depotentiated by stimulation on the negative phase in area CA1 in vivo. Journal of Neuroscience, 17, 6470-6477.
29. Kahana, M. J., Seelig, D., & Madsen, J. R. (2001). Theta returns. Current Opinion in Neurobiology, 11, 739-744.
30. Kaneko, T., & Thompson, R. F. (1997). Disruption of trace conditioning of the nictitating membrane response in rabbits by central cholinergic blockade. Psychopharmacology, 131, 161-166.
31. Larson, J., Wong, D., & Lynch, G. (1986). Patterned stimulation at the theta frequency is optimal for the induction of hippocampal long-term potentiation. Brain Research, 368, 347-350.
32. Lawson, V. H., & Bland, B. H. (1993). The role of the septohippocampal pathway in the regulation of hippocampal field activity and behavior: Analysis by the intraseptal microinfusion of carbachol, atropine, and procaine. Experimental Neurology, 120, 132-144.
33. Manns, J. R., Clark, R. E., & Squire, L. R. (2000). Awareness predicts the magnitude of single-cue trace eyeblink classical conditioning. Hippocampus, 19, 181-186.
34. Maren, S., DeCola, J. P., Swain, R. A., Fanselow, M. S., & Thompson, R. F. (1994). Parallel augmentation of hippocampal long-term potentiation, theta rhythm, and contextual fear conditioning in water-deprived rats. Behavioral Neuroscience, 108, 44-56.
35. Markowska, A., Olton, D., & Givens, B. (1995). Cholinergic manipulations in the medial septal area: Age-related effects on working memory and hippocampal electrophysiology. Journal of Neuroscience, 15, 2063-2073.
36. McEchron, M. D., & Disterhoft, J. F. (1999). Hippocampal encoding of non-spatial trace conditioning. Hippocampus, 9, 385-396.
37. Meador, K. J., Thompson, J. L., Loring, D. W., Murro, A. M., King, D. W., Gallagher, B. B., et al. (1991). Behavioral state-specific changes in human hippocampal theta activity. Neurology, 41, 869-872.
38. Mizumori, S. J. Y., Perez, G. M., Alvarado, M. C., Barnes, C. A., & McNaughton, B. L. (1990). Reversible inactivation of the medial septum differentially affects two forms of learning in rats. Brain Research, 528, 12-20.
39. Moyer, J., Deyo, R., Disterhoft, J. F. (1990). Hippocampectomy disrupts trace eye-blink conditioning in rabbits. Behavioral Neuroscience, 104, 243-252.
40. Myers, C. E., Ermita, B. R., Harris, K., Hasslemo, M., Solomon, P., & Gluck, M. A. (1996). A computational model of cholinergic disruption of septohippocampal activity in classical eyeblink conditioning. Neurobiology of Learning and Memory, 66, 51-66.
41. Oliver, C. G., Swain, R. A., & Berry, S. D. (1993). Hippocampal plasticity during jaw movement conditioning in the rabbit. Brain Research, 608, 150-154.
42. Pavlides, C., Greenstein, Y. J., Gudman, M., & Winson, J. (1988). Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of theta rhythm. Brain Research, 439, 383-387.
43. Prokasy, W. F. (1972). Developments with the two-phase model applied to human eyelid conditioning. In A. H. Black & W. F. Prokasy (Eds.), Classical conditioning: 11. Current research and theory (pp. 119-147). New York: Appleton-Century-Crofts.
44. rd ed., pp. 287-318). Hillsdale, NJ: Erlbaum.
45. Raghavachari, S., Kahana, M. J., Rizzuto, D. S., Caplan, J. B., Kirschen, M. P., Bourgeois, B., et al. (2001). Gating of human theta oscillations by a working memory task. Journal of Neuroscience, 21, 3175-3183.
46. Redish, A. D. (2001). The hippocampal debate: Are we asking the right questions? Behavioural Brain Research, 127, 81-98.
47. Salvatierra, A. T., & Berry, S. D. (1989). Scopolamine disruption of septo-hippocampal activity and classical conditioning. Behavioral Neuroscience, 103, 715-721.
48. Schmajuk, N. A., & DiCarlo, J. J. (1992). Stimulus configuration, classical conditioning, and hippocampal function. Psychological Review, 99, 268-305.
49. Schmaltz, L. W., & Theios, J. (1972). Acquisition and extinction of a classically conditioned response in hippocampectomized rabbits (Oryctolagus cuniculus). Journal of Comparative and Physiological Psychology, 79, 328-333.
50. Seager, M. A., Johnson, L. D., Chabot, E. S., Asaka, Y., & Berry, S. D. (2002). Oscillatory brain states and learning: Impact of hippocampal theta-contingent training. Proceedings of the National Academy of Sciences, USA, 99, 1616-1620.
51. Singer, W. (1993). Synchronization of cortical activity and its putative role in information processing and learning. Annual Review of Physiology, 55, 349-374.
52. Solomon, P. R., & Moore, J. W. (1975). Latent inhibition and stimulus generalization of the classically conditioned nictitating membrane response in rabbits (Oryctolagus cuniculus) following dorsal hippocampal ablation. Journal of Comparative and Physiological Psychology, 89, 1192-1203.
53. Solomon, P. R., Van der Schaaf, E., Thompson, R. F., & Weisz, D. (1986). Hippocampus and trace conditioning of the rabbit's classically conditioned nictitating membrane response. Behavioral Neuroscience, 100, 729-744.
54. Tesche, C. D., & Karhu, J. (2000). Theta oscillations index human hippocampal activation during a working memory task. Proceedings of the National Academy of Sciences, USA, 97, 919-924.
55. Thomas, M. J., Watabe, A. M., Moody, T. D., Makhinson, M., & O'Dell, T. J. (1998). Postsynaptic complex spike bursting enables the induction of LTP by theta frequency synaptic stimulation. Journal of Neuroscience, 18, 7118-7126.
56. Thompson, L. T., Moyer, J. R., & Disterhoft, J. F. (1996). Trace eyeblink conditioning in rabbits demonstrates heterogeneity of learning ability both between and within age groups. Neurobiology of Aging, 17, 619-629.
57. Thompson, R. F., Berry, S. D., Rinaldi, P. C., & Berger, T. W. (1979). Habituation and the orienting reflex: The dual process revisited. In H. D. Kimmel, E. H. Van Olst, & J. F. Orlebeke (Eds.), The orienting response in human (pp. 21-60). Hillsdale, NJ: Erlbaum.
58. Tracy, A. L., Jarrard, L. E., & Davidson, T. L. (2001). The hippocampus and motivation revisited: Appetite and activity. Behavioural Brain Research, 127, 13-23.
59. Vanderwolf, C. H. (1971). Limbic-diencephalic mechanisms of voluntary movement. Psychological Review, 78, 83-113.
60. Vertes, R. P., Albo, Z., & Viana Di Prisco, G. (2001). Theta-rhythmically firing neurons in the anterior thalamus: Implications for mnemonic functions of Papez's circuit. Neuroscience, 104, 619-625.
61. Wallenstein, G. V., Eichenbaum, H. B., & Hasselmo, M. E. (1998). The hippocampus as an associator of discontiguous events. Trends in Neurosciences, 21, 317-323.
62. Winson, J. (1978, July 14). Loss of hippocampal theta rhythm results in spatial memory deficit in the rat. Science, 210, 160-163.
63. Woodruff-Pak, D. S. (1999). New directions for a classical paradigm: Human eyeblink conditioning. Psychological Science, 10, 1-3.